Investigation of Musicality in Birdsong

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Hearing Research 308 (2014) 71e83

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Hearing Research

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Review Investigation of musicality in birdsong

David Rothenberg a, Tina C. Roeske b, Henning U. Voss c, Marc Naguib d, Ofer Tchernichovski b, * a Department of Humanities, New Jersey Institute of Technology, University Heights, Newark, NJ 07102, USA b Department of Psychology, Hunter College, City University of New York, New York, NY 10065, USA c Department of Radiology, Citigroup Biomedical Imaging Center, Weill Cornell Medical College, New York, NY 10021, USA d Behavioural Ecology Group, Animal Science Department, Wageningen University, Wageningen, The Netherlands article info abstract

Article history: Songbirds spend much of their time learning, producing, and listening to complex vocal sequences we Received 2 February 2013 call songs. Songs are learned via cultural transmission, and singing, usually by males, has a strong impact Received in revised form on the behavioral state of the listeners, often promoting affiliation, pair bonding, or aggression. What is it 7 August 2013 in the acoustic structure of birdsong that makes it such a potent stimulus? We suggest that birdsong Accepted 28 August 2013 potency might be driven by principles similar to those that make music so effective in inducing Available online 11 September 2013 emotional responses in humans: a combination of rhythms and pitchesdand the transitions between acoustic statesdaffecting emotions through creating expectations, anticipations, tension, tension release, or surprise. Here we propose a framework for investigating how birdsong, like human music, employs the above “musical” features to affect the emotions of avian listeners. First we analyze songs of thrush nightingales (Luscinia luscinia) by examining their trajectories in terms of transitions in rhythm and pitch. These transitions show gradual escalations and graceful modifications, which are comparable to some aspects of human musicality. We then explore the feasibility of stripping such putative musical features from the songs and testing how this might affect patterns of auditory responses, focusing on fMRI data in songbirds that demonstrate the feasibility of such approaches. Finally, we explore ideas for investigating whether musical features of birdsong activate avian brains and affect avian behavior in manners comparable to music’s effects on humans. In conclusion, we suggest that birdsong research would benefit from current advances in music theory by attempting to identify structures that are designed to elicit listeners’ emotions and then testing for such effects experimentally. Birdsong research that takes into account the striking complexity of song structure in light of its more immediate function e to affect behavioral state in listeners e could provide a useful animal model for studying basic principles of music neuroscience in a system that is very accessible for investigation, and where developmental auditory and social experience can be tightly controlled. This article is part of a Special Issue entitled . Ó 2013 Elsevier B.V. All rights reserved.

1. Introduction provides widely used textbook examples. Many studies have shown that singing behavior in most species has a dual function by Birdsong is among the most striking vocal displays in nature and attracting females and by serving as a territorial signal to keep out among the best studied communication systems in animals rivals (Catchpole and Slater, 2008). Yet, it is not entirely clear why (Catchpole and Slater, 2008). Juvenile songbirds acquire their songs birds sing in such complex ways (Rothenberg, 2005; Mathews, by imitating songs of adults. Usually only males sing but in some 2001), and the amazing diversity in birdsong still raises questions tropical birds both sexes sing duets in complex and melodious ways with respect to the features that make it such an important bio- (Thorpe, 1972). Birdsong has provided a useful model system for logical stimulus. Most research on birdsong emphasizes its ultimate vocal learning through research in ecology, animal behavior, function rather than its structure. However, the vast differences in neuroscience, physiology, psychology and linguistics and thus the length and complexity of species-speciﬁc songs cannot be easily explained in terms of functions like territory defense and mate attraction. As much as we know, the functions are by and large the * Corresponding author. Tel.: 1 646 5921240. same between species or individuals of a species, so why are the þ E-mail address: [email protected] (O. Tchernichovski). structural qualities so different?

Much of the research into song structure has been content with et al., 2005; Jarvis, 2007), and possibly even rely on similar genetics accepting the signal structure as largely arbitrary (which is, of (reviewed by White, 2010). course, compatible with Darwinian processes including sexual se- However, the limitations of the language-birdsong comparisons lection). Classifying song syllables into arbitrary indiscriminate are obvious, since birdsong lacks the semantics of language with its types followed by analysis of the statistical structure of those types mapping of combinable syntactical elements on accordingly com- has proven reasonable and useful. Based on this approach, in many bined meaning (for reviews, see Berwick et al., 2011, 2012). Note species stable song types have been identified as production units that contrary to birdsong, the bird sounds classified as “calls” often so that repertoire sizes can be quantified (Catchpole and Slater, have specific meanings, like “I’m hungry,”“Get away from my nest” 2008). Statistical song characteristics such as repertoire size, or “Watch out everyone, there’s a predator overhead” (see Marler, singing versatility and production of specific song components 2004, for a review). These usually innate sounds are much closer have indeed been identified as salient to avian listeners (Catchpole, to linguistic utterances than songs because they refer to specific 1980; Forstmeier et al., 2002; Hasselquist et al., 1996; Kunc et al., messages (although they don’t seem to be combinatorial like lan- 2005; Naguib et al., 2002; Podos, 1996; Podos et al., 2009) and as guage units; Hurford, 2011). In contrast, the songs of birds are functionally relevant (Catchpole, 1983; Kipper and Kiefer, 2010; repeated over and over again, like human songs. They are organized Naguib et al., 2011). While this statistical analysis of type classifi- formal performances with a typical beginning, middle, and an end. cation has its uses, it tends to deflect analysis away from the formal The very structure, form, inflection, and shape of birdsongs are relationship of adjacent types (i.e., notes or phrases) to each other. If independent of both a concrete message or an ultimate function, birdsong and music share similar mechanisms in affecting the which is reminiscent of human music and, indeed, it is not likely a behavioral state of the listeners, such statistical features would not coincidence that so many human languages call such sounds of reveal much of it: first order statistical features of music (e.g., birds “songs,” distinguishing them from the more speech-like calls. number of note types) have little to do with how music can evoke Further parallels between birdsong and music exist: 1) Humans emotion (see also Huron, 2006; Sloboda, 2005; Egermann et al., find listening to music rewarding and are willing to spend time and 2013). Instead, it is more likely to be the dynamic structure, e.g., money to hear it. Likewise, birds are attracted by birdsong and take the building up an arc of suspense, confirming or violating the some effort to hear it (Adret, 1993; Eriksson and Wallin, 1986; expectations of the listener, forming phrases containing a typical Gentner and Hulse, 2000; Riebel, 2000). 2) Like human musi- beginning, middle, or end, which make it work (Huron and Ollen, cians, birds distinguish between performing their song for others 2003; Meyer, 1956; Ng, 2003). Similarly, consideration of bird- (directed song) and practicing for themselves (undirected song) song structure dynamicsdfor instance, how its rhythms or pitch (Dunn and Zann, 1997; Hall, 1962; Morris, 1954a,b): directed song is intervals unfold through timedmay reveal important aspects of its behaviorally different (often accompanied by dance, faster, more effects on the behavioral states of listeners. Further, for humans and stereotyped) and relies on different brain activation and dopamine possibly also for birds it is much easier to remember a melody than release patterns (Hara et al., 2007; Jarvis et al., 1998; Kao et al., a random collection of notes (Deutsch, 1980). Such dynamic fea- 2008; Sakata et al., 2008; Sasaki et al., 2006; Stepanek and tures might bind together several song elements into a cohesive Doupe, 2010). 3) Birdsongs are transmitted vertically from parent percept. This might allow listeners to quickly assess a performance: to offspring as well as horizontally (between individuals of a pop- otherwise a common nightingale (Luscinia megarhynchos) would ulation), leading to regional dialects that are subject to cultural need to listen to a male song for about an hour to assess its full song evolution (Feher et al., 2009; Soha and Marler, 2000; West and repertoire (Hultsch and Todt, 1981; Kunc et al., 2005; Kipper et al., King, 1985). This is paralleled by regional musical traditions and 2006) and to compare several males would need to do so multiple cultural evolution of musical styles. times to assess each one’s repertoire size. Yet, prospecting males Despite these numerous similarities, there have been fewer and females initially spend very short periods near singers comparisons of birdsong structure to the structure of human music (Amrhein et al., 2004; Roth et al., 2009), suggesting that they than language (Araya-Salas, 2012; Baptista and Keister, 2005; quickly manage to extract principle features of the singing perfor- Dobson and Lemon, 1977; Fitch, 2006; Gray et al., 2001; mance. On the side of the singers, focusing on such features makes Hartshorne, 2008; Kneutgen, 1969; Marler, 2001; Slater, 2001; sense for another reason: singing often happens in a noisy Taylor, 2013; Tierney et al., 2011); attempts have sometimes been communication network where singers compete for attention by met with skepticism (see for instance Benitez-Bribiesca, 2001, and females (McGregor and Dabelsteen, 1996; Naguib et al., 2011). Song responses to Gray et al., 2001). A reason for this could be that must therefore be designed to proximately attract and maintain the musicality is a highly subjective concept. There are no simple attention of its receivers, which the singers might achieve by quantifiable measures of musicality that can be extended across manipulating rhythmic timing, amplitude, or other features. species. In fact, given that humans can make today music out of noises, gestures, patterns and textures, it has become hard to even 2. Human sounds and bird sounds: how birdsong, bird calls, find definitions that encompass only the total of human musicality. language, and music are related Not all music has a regular “beat” (birdsong rarely does) and only some music is based on regular sets of pitches known as scales. In recent research, structural aspects of birdsong have more Instead of deriving formal concepts from western music, trying routinely been compared to human speech and language than to identify these predefined concepts in the songs of different birds, music (Abe and Watanabe, 2011; Berwick et al., 2012; Bloomfield and then attempting to judge categorically if birdsong is musical or et al., 2011; Bolhuis et al., 2010; Fitch, 2011; Gentner et al., 2006, not, we can ask more generally how overall patterns in birdsong, 2010; van Heijningen et al., 2009; Lipkind et al., 2013; Margoliash including dynamic transitions from the expected to the unex- and Nusbaum, 2009, to just name a few). This might be so pected, may affect a bird’s behavioral state and the behavioral state because both share the striking and rare trait of vocal learning of its listeners. The proximate function of driving emotional re- through the acquisition of complex vocal sequences by sensorye sponses through complex, structured, non-sematic sound streams motor integration processes through practice early in life (Doupe might be a powerful parallel between music and birdsong. We and Kuhl, 1999), involve homologous brain structures (Jarvis expect that their structures would be shaped by and could be un- et al., 2005; Jarvis, 2007) such as a specialized telencephalice derstood in terms of the function of driving emotional responses, as basal gangliaethalamic loop (Brenowitz and Beecher, 2005; Doupe is assumed for music (Huron, 2006; Meyer, 1956) and has been D. Rothenberg et al. / Hearing Research 308 (2014) 71e83 73

Fig. 1. Olavi Sotavalta’s nightingale song analysis (Sotavalta, 1956). A, Generalized musical structure of each phrase. B, Excerpts from his catalog of all the phrases sung by his two study birds. C, Analysis of sequence of phrases in the nightingale song, showing a loosely patterned progression through the repertoire. 74 D. Rothenberg et al. / Hearing Research 308 (2014) 71e83 proposed for birdsong (reviewed by Riters, 2011). If this is true, it enough to avoid introducing human-music-centric (or even worse, might become practical to use current techniques in music theory western-music-centric) paradigms and biases into the analysis. to design cross-species experiments. Then, we discuss methods for testing whether putative musical However, current measures of structural aspects of birdsong are features of the song activate neural loci and affect behavioral of limited use when it comes to investigating how song might drive states in birds in a manner that is comparable to how music ac- its listeners’ emotions. For example, showing that a male bird with tivates human brains and affects human behavior. the most number of syllables or the most complicated song has more mating success may work, but only in a small number of 4. Searching for sound structures that have “emotive power” species, including the sedge warbler (Catchpole, 1980; Catchpole and Slater, 2008). It is therefore desirable to find a more nuanced When trying to identify which aspects of birdsong make it a but quantifiable esthetic sense that could work in species with powerful emotion-manipulator, our own esthetic sense may be more complex and refined songs such as nightingales, butcher- useful as a first guide: humans are attracted to the songs of many birds, thrashers, wrens and mockingbirds. As in human music, the bird species and often find them musical, organized, and estheti- most and the loudest is not always the best. As Darwin noted in a cally pleasing. Many species’ songs are characterized by a mixture letter to Asa Gray, “birds have a natural esthetic sense. That is why of clearly-pitched whistle tones, rhythmic clicks and buzzes. they appreciate beautiful sounds.” What are the sounds most Consecutive pitch intervals tend to differ in direction, in marked beautiful to each species? We should strive to measure that. contrast to what is most common in human music (unpublished observation in European nightingale song). Human listeners who 3. A history of birdsong aesthetics hear nightingale songs for the first time after having read of them in classical European literature are often surprised that they sound Ours is by no means the first plea for a more esthetic approach to not quite like the pure melodies one would expect to be so cele- making sense of birdsong. One of the most interesting attempts to brated by Keats, Wordsworth, and John Clare (Rothenberg, 2005). apply musicological terminology to birdsong came from the pro- The beauty and power we perceive when listening to a nightingale cess philosopher Charles Hartshorne (Hartshorne, 1973). Based on singing on sunset comes in part from its otherworldly qualities. qualitative observations, he proposed that nearly every conceivable When targeting structural features of birdsong for analysis, attribute of human music exists somewhere in the songs of birds: predetermining any particular feature bears the risk that this very accelerando in the field sparrow (Spizella pusilla) and ruffed grouse feature might not play a major role in the esthetics of a particular (Bonasa umbellus) and ritardando in the yellow-billed cuckoo bird species in question. A reasonable starting point would be to (Coccyzus americanus); crescendo in Heuglin’s robin chat (Cossypha first look for any structure that is stereotyped but allows for some heuglini) of Africa and diminuendo in the Misto yellowfinch (Sicalis degree of variation. Such structures would be good candidates to luteola) of South America; harmonic relations in the crested bell- generate expectations in avian listeners, with which comes the bird (Oreoica gutturalis) of Australia and the warblers of Fiji; and possibility of predictions, anticipations, delays, or surprises, which themes and variations in the Bachman’s sparrow (Peucaea are believed to underlie the “emotive power” of human music aestivalis). (Huron, 2006; Meyer, 1956): recurring stereotyped structures will The most complex birdsongs often include many such musical create in listeners an anticipation of what to expect next, which can elements in a single song. Below, we present sonograms of thrush be fulfilled (leaving the listener with a sense of satisfaction), nightingale songs that illustrate this (Fig. 2). Similar analyses were delayed (first increasing tension that gives way to an increased made by Olavi Sotavalta, who made diagrams of the thrush night- degree of satisfaction) e or violated (creating surprise). Stereotyped ingale’s(Luscinia luscinia) song that resemble our sonograms but yet varied structures can occur on all hierarchical levels: single using modified musical terminology instead (Fig. 1A; Sotavalta, notes (or subphrases of a few notes) can be repeated but modified 1956). slightly in timing or amplitude, for example, and entire phrases can Sotavalta segmented the bird’s many phrases and musically occur repeatedly within a single performance with subtle varia- notated them (Fig. 1B) before analyzing their sequence and tions in the order of some notes (as in European Nightingales). concluding that the bird went through his phrases in a loosely Contrast between adjacent materials e like for spectral differences patterned order (Fig. 1C). There was a sense of a periodic progres- between the mockingbird’s successive phrase groups e are also sion through the repertoire but no sequence of riffs was precisely thought to be a source of emotions evoked in the human listener the same as the next. Sotavalta’s approach is an interesting hybrid (Huron, 2006). Such contrasts in birdsong, be it in the rhythmic, between musical notation and quantitative statistical thinking. spectral, or dynamic domain, might be quantifiable and its use can While he wasn’t able to do multivariate statistical analysis yet, he be tracked across performances. We are presenting here an analysis developed hybrid visualizations that would make sense to musi- of thrush nightingale songs in which contrast and variation become cians, with their sense of sound and order unfolding through time. visually graspable. Once such putatively musical features of a spe- Since then, there have been only a handful of studies that consider cies’ song are identified, they can be tested for their emotive power: the musicality of complex birdsongs (Baptista and Keister, 2005; if avian listeners are presented with song samples containing these Brumm, 2012; Craig, 1943; Dowsett-Lemaire, 1979a,b; Earp and features versus song samples stripped of these features, the emo- Maney, 2012). tions elicited, and therefore their neural activation patterns, should Are these merely subjective evaluations or is this a window differ if the feature in question is indeed biologically relevant to the onto a species-wide nightingale esthetic? Here we propose a bird. We will argue here that one potentially successful method for simple framework for investigating how the statistical structure of detecting differential emotive power is functional magnetic reso- birdsongs can be described in terms that are not foreign to mu- nance imaging (fMRI). sicians, and then address the functional question of identifying which structural aspects affect a bird-listener’s behavior. To ach- 5. A case study: assessing “musical” structure of the thrush ieve that, we will need to develop descriptive models of birdsong nightingale song that are compatible with human music, including representations of pitch intervals and of rhythms that could reveal patterns of Here we present a case study in which we developed a rhythmic timing, melodic course, etc. The approach is generic descriptive model of thrush nightingale songs that captures its D. Rothenberg et al. / Hearing Research 308 (2014) 71e83 75

Fig. 2. Time structure of the song. A, One song motif with syllable outlines in dark red; B, phase plot of onset-to-onset time intervals for an entire performance. Each dot represents a syllable in its rhythm context, i.e. its temporal relation to the previous and the following syllable’s onset. We call this a rhythm unit. Clusters indicate specific rhythm units that are recurring throughout the bird’s performance; C, each song can be plotted as a trajectory in this phase plot, propagating from one rhythm structure into the next. D. Continuous escalation of the rhythm during the first part of the motif, curve indicates onset-to-onset intervals for pairs of downsweeps while spectral bandwidth increases; E, subtle escalation of amplitude during a trill of clicks leading to the next motif whistle. putatively musical features. Thrush nightingales are among the neighbors later on in life also occurs (Griessmann and Naguib, most melodious singers, with large repertoires and versatile 2002; Sorjonen, 1977). Studies in its sibling species, the Common singing styles. The song of the thrush nightingale, found in Nightingale, showed that some song elements appear to be Northern and Eastern Europe, is impressive: males often sing improvised (Hughes et al., 2002). Renditions of the same song type almost continuously for several hours, starting in the evening and are often not identical, with subtle variations in the structure and continuing into the night (Naguib and Todt, 1998; Naguib and Kolb, number of elements and in rhythm. 1992). They usually produce 15e20 different song types, often with We used audio recordings from two thrush nightingales who many intermediate variants, delivered in variable order. Males sang naturally in the field. Recordings were made at the Island learn those songs in their first year but some learning from Hiddensee in Northern Germany in 1996 (Naguib and Todt, 1998). 76 D. Rothenberg et al. / Hearing Research 308 (2014) 71e83

For each bird we used 30e50 min of continuous nocturnal singing. next syllable, which is a high pitch sweep that terminates the song, Male thrush nightingales sing at night over several hours, pre- like a glissando in music. Note that in both cases, a subtle gradual sumably until they attract a social mate for breeding as shown for change (acceleration in phrase 2, amplitude increase in phrase 3) their sibling species, the nightingale (Amrhein et al., 2002). can be interpreted as preparing for and bridging a phrase bound- We then analyzed the entire singing behavior recorded for each ary: the acceleration in phrase 2 leads over to an ever faster rhythm bird (about 50,000 song syllables per bird). Using the Sound in phrase 3, and the increasing amplitude in phrase 3 culminates in Analysis Pro 2011 software (SAP2011, Tchernichovski et al., 2000; the note of phrase 4. Is this way of linking different phrases part of a SoundAnalysisPro.com), we performed multi-taper spectral anal- thrush nightingale aesthetics e i.e., does it elicit emotions and ysis (FFT window 8 ms, bandwidth parameter 1.5, overlap 7 ms) expectations, like the build-up of tension that releases when the and computed spectral derivatives (high-definition sonogram im- phrase boundary is reached? We will later suggest an approach to ages). We automatically segmented the song data into syllables such questions using functional brain imaging in avian listeners. using an adaptive amplitude threshold (recorded amplitude filtered Note that a symbolic description of these songs, namely, cate- with a HodrickePrescott filter set to 400 samples, as implemented gorizing syllable types and phrase types (essentially, what all pre- in SAP2011). We identified syllables (versus inter-syllable silence) vious studies have done in stage 1 of the analysis), does not take as all sound where amplitude (filtered with a HodrickePrescott into account the subtle transitions we described above. Yet, filter set to 50 samples) exceeded the threshold. Mean values of removing these transitions from the signal makes it sound very song features, including mean frequency and Wiener entropy, were different. According to Juslin (Juslin and Västfjäll, 2008; Juslin and computed for each syllable and saved in MySQL tables. Data were Sloboda, 2010), in human music, what communicates emotion further analyzed using Matlab 7 (The Matworks, Inc., Natnick, MA) may not be melody or rhythm as exactly noted in the sheet but and Microsoft Excel 2011 (Microsoft, Inc., Seattle, WA). moments when musicians make subtle changes to those musical patterns. “Musicality” is a combination of all these elements of 5.1. Analysis of thrush nightingale song time structure rhythm, melody, form, dynamics, timbre, and inflection. Perhaps birdsong, as in human music, combines these into coherent The building blocks of the thrush nightingale song are phrases of species-specific wholes. Stripping such subtleties from birdsong repeated syllables. Whereas Sotavalta used his own ear in musical could affect neuronal and behavioral responses but such effects notation and in manual enumeration of patterns, it is now techni- have not been tested in birds, though they have in humans (Chapin cally feasible to visualize patterns in the raw song data in a manner et al., 2010). that is compatible with his ideas. In Fig. 2A we present spectral derivatives of one song composed of four phrases: the first is a 5.2. Is exploring pitch space a matter of individual skill? single syllable followed by a phrase of several down-sweeps which are delivered in pairs (chipechip, chipechip.), a third phrase A recent paper on the possibility of musical scales in the tonal- composed of clicks, which are delivered in quartos, and a final sounding song of the Northern nightingale wren (Microcerculus single syllable. While the sonogram image clearly shows this coarse philomela) concludes that there are no musical scales in those songs rhythmic structure, subtle modifications within these repetitive (Araya-Salas, 2012). Another study by Tierney et al. (2011), how- patterns, such as the slight acceleration in the second phrase, are ever, finds evidence that some of the elements of musical structure more difficult to see: this is a case where the singer adds a sys- are shared between humans and birds but those may be based on tematic variation in timing to an otherwise stereotypically repeated motor constraints on what possible sounds can be produced. Their note. This accelerando may possibly constitute a “musical” feature study compares musical scores of nearly 10,000 folk songs, mostly that is able to evoke emotions, expectations, and anticipation in European but also 2000 Chinese examples, with 80 species of thrush nightingale listeners. To capture such time structure, we birdsongs, hand-picking those that are primarily tonal with sig- analyzed the entire singing performance of one male during about nificant pitch variation. They purposely excluded birdsongs with 1 h of singing, including about 50,000 song syllables, and con- noises, clicks, buzzes, and other sounds difficult to notate musically. structed a phase plot of the onset-to-onset time intervals of song Within this subset of songs they determined that the relative syllables (Fig. 2B). While will call this temporal aspect of birdsong preference for consistency in melodic contour is remarkably similar “rhythm,” please note that we do not intend to imply the existence between birds and humans, as well as the fact that phrases tend to of an underlying beat maintained throughout a song. Each dot lengthen toward their conclusions. Both birds and humans also represents one syllable in its rhythmic context. It shows two time tend to favor smaller interval jumps rather than larger ones. The intervals: between a syllable and the onset of the previous syllable authors hypothesize, in conclusion, that physical motor constraints (X axis), versus the time interval to the next syllable (Y axis, e.g., the lead to this similarity. duration from syllable 1 to syllable 2 versus the duration from We are not sure what they would make of the songs of thrush syllable 2 to syllable 3). The clusters indicate that this bird sings nightingales, starlings, cowbirds, or lyrebirds that specialize in using about 20 different rhythmic units, although some of those are strange, glottal sounds and big contrasts between steady tones and harmonically related to each other (i.e., they represent versions of rapid ratchety beats or wide-frequency bursts of precisely the same rhythmic motif in different speeds that are small fractions controlled noises. Other researchers have pointed out that physi- or multiples of each other). Within these plots, each song can be cally the syrinx of birds is capable of far more sonic variation than represented as a trajectory in rhythm-space (Fig. 2C). For example, most birds make use of (Zollinger and Suthers, 2004), so that the by plotting the song presented in panel A we can see how the predilection for one species to have a far more complex song than rhythm zigzags during the phrase of down-sweeps and then orbits another has more to do with selective pressures on the species song into rapid three-state oscillations while performing the clicks. evolution than any physical limitation. Lyrebirds, which have one of This phase plot reveals a graceful transition from one rhythm the most complex and convoluted of all birdsongs, have a simpler state to the next: the zigzag pattern gradually accelerates until it syrinx than most songbirds (Robinson, 1991), yet they produce enters into the orbit of the click phrase. Fig. 2D shows a quantifi- songs of astonishing complexity. This is not to say that motor cation of this transition. Further, although the rhythm of the clicks constraints might not have some role in the fact that human and is very stable, another feature, in this case amplitude, increases bird music contains many similar features but motor constraints during the clicks phrase, slowly approaching the amplitude of the tell only one part of the story. Investigating the form of the D. Rothenberg et al. / Hearing Research 308 (2014) 71e83 77

Fig. 3. Songs depicted as trajectories through spectral space. A, An example of three consecutive songs produced by a thrush nightingale, each song including phrases of whistles and clicks. Below the sonogram, zooming in using spectral derivatives shows that the click trills include a complex fine structure, produced in sets of 4, 2 or 1, sometimes with low pitch whistles in between (second panel); B, to summarize an entire singing performance over about 1 h of continuous recording, we present a scatter plot of syllable features, where each dot represents the pitch versus Wiener entropy of one syllable; C, a trajectory of one song in this space. DeE, Same representation for a different bird. rhythmic, harsh phrases uttered by thrush nightingales as we have the birds’ songs themselves. Thrush nightingale syllables are rarely attempted here might complement the tonal and melodically- pure tones; instead, their syllables are usually frequency modulated expectant approach of Tierney, Russo, and Patel. whistles or clicks (Fig. 3A). However, zooming into the spectral Here we propose an alternative approach of exploring the space derivatives (Fig. 3A inserts) reveals that even the clicks may have a of tones and tonality more generally. As we did with analysis of more complex frequency and rhythm structure than the human ear rhythm, we examined songs as trajectories in that frequency space, first picks up. Therefore, we use two features to summarize their searching for musical features in those trajectories. As in our pre- frequency structure: one is the mean frequency of the syllable, liminary investigation of rhythm, the putative musicality we are which is an estimate of pitch. The other is Wiener entropy, which is positing in birdsong emerges through analysis of the structures of an estimate of tonality, ranging from white noise (high spectral 78 D. Rothenberg et al. / Hearing Research 308 (2014) 71e83 entropy) to pure tone (low spectral entropy). Note that we are using might be more useful to take some obvious commonalities between the term “tonality” here in the sense of “tone-like” as used in signal the two series and explore points of view that are more tradition- analysis as opposed to its use in music theory to denotes re- ally found in contemporary music theory. lationships of different tones on a scale. Fig. 3B presents a scatter plot of mean frequency versus Wiener entropy for an hour of 6. What music tickles bird brains? singing performance of one bird. As shown, the song is composed of distinct classes of vocal sounds: clicks of high Wiener entropy and Humans are consistently impressed by musicality heard in syllables composed of tonal elements with no overtones (whistle) birdsong. But are birds impressed by features humans perceive as or of low or high pitch. musical? Above, we presented an approach for detecting musical As for rhythm, we plotted each song as a trajectory in feature features of birdsong. How might we examine what these features space (Fig. 3C). Comparing two birds (Fig. 3B and D), we see that mean to the minds of the birds themselves? one bird (Fig. 3B) has more distinct classes of vocal sounds with We can look for activation of neuronal mechanisms and the significant gaps between them. The other bird, although having alteration of behavior by i) synthesizing songs that are stripped of similar categories of sounds, produces syllables that fill the feature those features (e.g., constructing thrush nightingale songs without space much more continuously, e.g., including many intermediate accelerations leading to transitions); ii) detecting homologous forms between clicks and low pitch whistles. Interestingly, song features in human music; and iii) comparing changes in brain trajectories of the first bird tend to be more linear, e.g., starting from activation and behavioral patterns across songbirds and humans a phrase of low pitched whistles followed by a phrase of clicks (as in when listening to the two original versus synthetic sounds. We Fig. 2A). The other bird, however, shows also circular trajectories, focus on the feasibility of the attempt to identify shared mecha- making complete cycles from a click to a low pitch whistle, high nisms by which sounds can alter behavior and for determining pitch whistle, and back to a click, such as the one shown in Fig. 3E. whether they are shared between birdsong and human music. In Do such transitions indicate virtuosity, suggesting that one of the humans, listening to an expressive performance of music activates birds exploits the pitch space more skillfully than the other bird? different brains centers than listening to a mechanical performance When focusing on musical features of birdsong, we have to assume of the same piece (Blood and Zatorre, 2001; Chapin et al., 2010). that eliciting in the listeners suspense, surprise, and pleasant ten- Such differences can be seen not only in auditory areas but also in sion release requires skill and that such musical skill differs be- reward and emotion-related areas such as the ventral striatum, tween individuals (just as it does between human musicians). How midbrain, amygdala, orbitofrontal cortex, and ventral medial pre- would avian listeners respond to synthetic playbacks of songs frontal cortex, as well as in motor and “mirror-neuron-” rich areas where the degree of pitch and entropy contrast is systematically (including bilateral BA 44/45, superior temporal sulcus, ventral altered, in a way similar to what is different between the songs of premotor cortex, inferior parietal cortex, insula). our two birds? Previous studies showed that birds will calibrate What features of birdsong activate brain centers and affect their performances when presented with song models that include behavior in a manner that might be comparable to human music? trills that are too fast for them to produce (Podos,1996) and females We will review and compare the literature about auditory re- find trills produced at the species’ performance limit as being more sponses to song in songbirds and how they resemble auditory re- attractive (Ballentine et al., 2004). Here, we suggest another way of sponses to music in humans. We then argue that methods allowing looking at complex performances, which is summarized in Figs. 2 direct comparative studies are already in place, focusing on recent and 3: first, present songs as trajectories in continuous rhythm fMRI studies in songbirds. Those demonstrate that non-invasive space and in frequencyeentropy space instead of using symbolic techniques can capture song-specific patterns of brain activation notations based on cumulative statistics. Then, explore entire per- which relate not only to acoustic structure but also to the social formances, looking for systematic variations between perfor- significance of the song and to the developmental history of the mances of different individuals or between one individual’s singing bird. Finally, we suggest a roadmap for combining these approaches in different social contexts. Some structures will be shared across and discuss the potential and difficulties of attempting direct all performances (e.g., the general tendency to alternate trains of comparisons between human and avian systems. clicks with trains of whistles in the case of the thrush nightingales). Note that fMRI is just one of many possible readouts for effects Such shared structures most likely reflect species-typical song of musical features on listeners’ brain and behavioral states, and a features that might be interpreted as a “default.” Systematic vari- number of possible alternatives are conceivable. Behavioral assays ations between individuals, on the other hand (such as the different like learning experiments can reveal preferences for certain use of entropy-frequency space of the two thrush nightingales musical features: a young bird who is acquiring his song can be shown), are what might carry information about virtuosity and presented with two models, one of which contains while the other thus affect a listener’s attention and response. Once variants are lacks the musical feature in question (in the same way as described identified, we can quantify the auditory and behavioral responses above). The bird will reveal his preference by copying one of the they elicit and create new variants with over- or under-emphasized models. Behavioral female choice experiments can tell what kind of distances to the default. These can be tested for auditory and song is preferred by female avian listeners. Electrophysiology can behavioral responses. What are we missing when looking at song be used to record brain responses to different song samples with symbolically? We are missing the transitions in acoustic space, high temporal resolution (although at the expense of a good spatial which are, to a large extent, what makes music work. The arbitrary resolution). An interesting technique to assess the role of dopamine naming of phrases or states (A, A1, B, C, etc.) does not reveal musical in the processing of such “musical” versus “non-musical” song structure. The analysis of analog features such as variations in stimuli are PET scans using radioactive dopamine antagonists: they amplitude and rhythm suggest musicality in the details of the song, can reveal whether the two kinds of stimuli lead to different perhaps generating tension and expectation in manners be com- amounts of dopamine released. We will here discuss in detail e as parable to human music. one possible option e fMRI, which with stronger (7T and 9T) This case study demonstrates that looking at a single species in scanners now becoming available, has the advantages of being a sufficient detail and considering continuous feature space may non-invasive brain imaging technique with a good spatial resolu- reveal acoustic attributes that are most meaningful to this species: tion even for small brains. However, the temporal resolution of instead of testing in general if music and birdsong are similar, it fMRI is orders of magnitude slower than short time scales in D. Rothenberg et al. / Hearing Research 308 (2014) 71e83 79

Fig. 4. Auditory responses in the zebra finch brain are stimulus specific. A, BOLD responses to different stimuli at the medial portion of right and left hemispheres in zebra finches; B, summary of BOLD effects across birds. TUT tutor’s song, BOS bird’s own song, CON a song of unfamiliar zebra finch, TONE a 2000 Hz tone. From Voss et al. (2007a,b). birdsong. In fMRI experiments, we are constrained to assessing the in song structure. However, most of the methods mentioned above time-averaged regional response of the brain to these modified were obtained by recording from single units or by analysis of gene stimuli. In this sense, it might be that a modified song activates expression patterns in brain areas after song playback. These ways other regions than the unmodified song, that the amplitude of of measuring neuronal responses are not directly comparable to activation systematically differs, or that the shape of the response studies of music and, in most cases, they involve acute or terminal over time changes with the stimulus. preparations. An alternative approach, which is more comparable Auditory responses to birdsong have been studied intensively, to human studies, uses non-invasive imaging techniques such as from auditory brainstem responses and activation by songs (Henry fMRI. Recent studies by our groups (Maul et al., 2010; Voss et al., and Lucas, 2008; Poirier et al., 2009) to investigations of song- 2007a,b, 2010) and by others (Boumans et al., 2005, 2007, specific responses in the auditory mid- and forebrain (Woolley 2008a,b; Peeters et al., 2001; Poirier et al., 2009, 2010, 2011; Van et al., 2005, 2006), in secondary auditory and integration areas Meir et al., 2003, 2005) showed that the specificity of auditory (NCM), and also in motor and sensoryemotor song nuclei (Chew responses to particular songs can be detected by looking at BOLD et al., 1995; Vicario and Yohay, 1993). The auditory representation responses. These fMRI studies show that, as in human music, brain of the song transforms from simple feature detectors in the activation in response to birdsong can be lateralized and strongly brainstem to complex, song-specific responses in higher brain areas depends on the social significance of song (Fig. 3): comparing BOLD (Woolley et al., 2005, 2006). There are strong auditory responses to responses to songs versus tones, there are significant differences songs in all the motor song nuclei (Doupe, 1997; Margoliash and only in the right hemisphere, with Bird’s Own Song (BOS) inducing Konishi, 1985), which are strongly modulated by behavioral state the strongest BOLD responses. The left hemisphere show strong (Cardin and Schmidt, 2003). Overall, the auditory responses to BOLD responses as well, but those are less stimulus-specific. Note, songs are strongly stimulus specific, depending on the overall time however, that all those studies were performed in a single species and frequency structure of the song. (zebra finches) (Fig. 4). Most remarkable are the auditory responses to the Bird’s Own Song (BOS): the song nuclei usually respond very strongly to 6.1. The development of auditory responses to songs playbacks of BOS compared to any other song (Doupe, 1997; Solis and Doupe, 1997). Even small acoustic modifications might suffice One issue that complicates musical analysis are the effects of to eliminate BOS specific responses (Theunissen and Doupe, 1998). development and culture, which is very difficult to segregate in Further, when the bird sings, corollary discharges of the premotor humans. Using songbirds as animal models for studying basic song patterns propagate into the anterior forebrain pathway, sug- mechanisms of music neuroscience could circumvent these gesting sensoryemotor mirroring (Mooney and Spiro, 1997; complicating factors: first, in songbirds auditory experience during Mooney et al., 2002). It is the same neurons in the song system development can be tightly controlled. Second, early auditory that can switch, within seconds, from premotor to auditory re- exposure has strong effects on the specificity of fMRI responses to sponses of very similar patterns (Prather et al., 2008). Therefore, songs, so that the effects of development and culture on auditory sensoryemotor auditory responses to birdsong are similar to sen- processing could be accessed with this technique. soryemotor responses to music in humans (Callan et al., 2006; To demonstrate this point we present data from our recent study Hickok et al., 2003; Pa and Hickok, 2008). As in humans, both comparing BOLD responses to two stimuli: playbacks of the bird’s auditory and motor song-related brain activity is lateralized (Cynx own song (BOS) versus a repeated song syllable (i.e., a simple re- et al., 1992; Espino et al., 2003; Floody and Arnold, 1997; George petitive song). Colony-raised birds show much stronger responses to et al., 2005; Halle et al., 2003; Hartley and Suthers, 1990; BOS, which is expected (Fig. 5A). However, this stimulus-specific Moorman et al., 2012; Nottebohm, 1971, 1972; Phan and Vicario, response depends on early experience and perhaps also on normal 2010; Remage-Healey et al., 2010; Van der Linden et al., 2009; song development: in birds that were raised in complete social and Voss et al., 2007b; Williams et al., 1992). auditory isolation during the sensitive period for song learning we This evidence indicates that auditory responses to song play- see strong responses to both stimuli (Fig. 5B). Comparing several backs are specific enough to test the effect of subtle manipulations stimuli, including the tutor song (TUT), conspecific song (CON), and 80 D. Rothenberg et al. / Hearing Research 308 (2014) 71e83 tones across several birds (Fig. 5C and D), we can see that this effect One conceptual difficulty in comparing auditory responses be- generalizes. We conclude that the auditory responses are specificto tween birdsong and human music is that there is no simple way to songs of different social significance (keep in mind that the partic- distinguish auditory responses to music and auditory responses to ular BOS and TUT songs are different in each bird) and that this other natural sounds. There is no simple answer to this question stimulus specificity is therefore an outcome of early experience. because the perception of music is, to a large extent, built upon Since BOLD responses reveal these experience-based effects they are natural time scales of responses to stimuli we have evolved to a promising means to explore the subtle differences between songs respond to. However, in order for music to “work” it must meet that have been musically manipulated (such as containing versus some conditions: first, there should be some balance between being stripped off timing subtleties, as in Fig. 2). anticipation and suspense; otherwise, the music would become boring or incomprehensible (for discussion see Huron, 2006). 6.2. Challenges in comparative studies of music and birdsong Second, music has a strong sensoryemotor aspect: this is true not only for musicians, who can often inverse the perception of music The results above suggest that the gap between birdsong into motor gestures, but also for non-musicians, who perceive research and human music neuroscience research might be some aspects of the music via their motor system (Haueisen and bridgeable. Of particular interest is a direct comparison when some Knösche, 2001). The association between music and movement aspects of the musical features are removed and when listeners’ can explain some of its power in driving emotion, namely, by brain activation patterns are analyzed as they listen to music activating motor centers that are associated with different types of stripped of dynamic variation, expression, and other emotionally- actions (i.e., motor correlates of marching, having sex, or feeling evoking acoustic features (Chapin et al., 2010). A parallel study in weakness). Finally, the perception of music has a strong develop- thrush nightingales would include subtle adjustment of the dy- mental component and people from different cultures might differ namics and micro-tempo (acceleration) of phrases, similar to those in some very basic perceptual aspects of music including the no- shown in Figs. 2 and 3. One can then use fMRI as in Voss et al. tions of consonance and dissonance, time scales and rhythms. As (2010), perhaps in addition using heart rate as a proxy for elaborated above, all those aspects can be found in birdsong, changes in internal state. including studies showing that female song preference are shaped

Fig. 5. Auditory responses depend on developmental experience. A, BOLD responses in colony raised birds show strong differences comparing the bird’s own song (BOS) to a repeated syllable, but not in isolate males. B, A summary across stimuli shows stimulus specific responses only in colony raised males, but not in isolate males, whose responses are highly variables. From Maul et al. (2010). D. Rothenberg et al. / Hearing Research 308 (2014) 71e83 81 by the early developmental conditions (Holveck and Riebel, 2010; Acknowledgments Riebel et al., 2009). However, to show that birdsongs are truly musical one must be able to find specific features of performance We thank E. Janney for comments and suggestions. Supported that, independently from the coarse song structure, may affect by NSF award 1261872 to OT & HV and by NIH award PHS DC04722 behavioral responses in an interesting and functionally relevant to OT. manner. There is no empirical evidence for the emotive power of specific features of the song but Earp and Maney (2012) were able to show that the same reward related brain circuit that is active in References humans listening to music e the mesolimbic reward pathway Abe, K., Watanabe, D., 2011. Songbirds possess the spontaneous ability to discrim- (Blood and Zatorre, 2001; Koelsch et al., 2006; Mitterschiffthaler inate syntactic rules. Nat. Neurosci. 14, 1067e1074. et al., 2007; Montag et al., 2011; Pereira et al., 2011; Salimpoor Adret, P., 1993. Operant-conditioning, song learning and imprinting to taped song in fi et al., 2011) e is activated in birds listening to birdsong. The the zebra nch. Anim. Behav. 46, 149e159. Amrhein, V., Korner, P., Naguib, M., 2002. Nocturnal and diurnal singing activity in approach we suggest here e presenting avian listeners with more the nightingale: correlations with mating status and breeding cycle. 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